Skip to main content
SpringerLink
Log in

Prediction of the Mannose-Binding Site in the Agaricus bisporus Mannose-Binding Protein

  • Published:
The Protein Journal Aims and scope Submit manuscript

Abstract

Agaricus bisporus mannose-binding protein (Abmb) was discovered as part of mushroom tyrosinase (PPO3) complex. Apart from its presence, nothing is known about its function or activity in the mushroom. The protein is evolutionarily related to lectins with β-trefoil fold, which are glucose or galactose (and their derivatives) binding proteins. Abmb is also recently showed to display the typical agglutination activity of lectin when in complex with PPO3; this further supports Abmb similarity to its structural homologs from lectin with β-trefoil fold. However, Abmb has no affinity towards glucose or galactose but for mannose, thus its binding to the sugar may be different from its homologs. To date, the natural ligand of Abmb is unknown and the structure of Abmb in the presence of a ligand is not available. Therefore, the mannose-binding site of Abmb was predicted using molecular docking, which was consulted with the information from its structural homologs. This conservative approach would prevent over-speculation. The mannose-binding site of Abmb is likely located in the same region to that of Abmb structural homologs but with a shift in position due to the presence of additional surface loop. In addition, benefiting from the information from an in vitro study on Abmb sugar specificity, the mannose poses suggested that the sugar might interact with the side chains of Arg15, Thr45, Gln48, Asp49, Asp51 and Arg51. Most of these residues were equally present in Abmb structural homologs despite variation of their positions in the amino acid sequence. The variation probably originates from alteration of its amino acid sequence during evolution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Abbreviations

DLD:

N-N’-di-acetyl-lactosediamine

PPO:

Polyphenol oxidase

RBC:

Red blood cells

RMSD:

Root mean square deviation

References

  1. Ismaya WT, Rozeboom HJ, Weijn A, Mes JJ, Fusetti F, Wichers HJ, Dijkstra BW (2011) Crystal structure of Agaricus bisporus mushroom tyrosinase: identity of the tetramer subunits and interaction with tropolone. Biochemistry 50(24):5477–5486

    Article  CAS  PubMed  Google Scholar 

  2. Ismaya WT, Rozeboom HJ, Schurink M, Boeriu CG, Wichers H, Dijkstra BW (2011) Crystallization and preliminary X-ray crystallographic analysis of tyrosinase from the mushroom Agaricus bisporus. Acta Cryst F 67:575–578

    Article  CAS  Google Scholar 

  3. Weijn A, Bastiaan-Net S, Wichers HJ, Mes JJ (2013) Melanin biosynthesis pathway in Agaricus bisporus mushrooms. Fungal Genet Biol 55:42–53

    Article  CAS  PubMed  Google Scholar 

  4. Ismaya WT, Tjandrawinata RR, Dijkstra BW, Beintema JJ, Nabila N, Rachmawati H (2020) Relationship of Agaricus bisporus mannose-binding protein to lectins with a β-trefoil fold. Biochem Biophys Res Commun 527:1027–1032

    Article  CAS  PubMed  Google Scholar 

  5. Sayadmanesh A, Ebrahimi F, Hajizade A, Rostamian M, Keshavarz H (2013) Expression and purification of neurotoxin-associated protein HA-33/A from Clostridium botulinum and evaluation of its antigenicity. Iran Biomed J 17(4):165–170

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Svajger U, Pohleven J, Kos J, Strukelj B, Jeras M (2011) CNL, a ricin-B like lectin from mushroom Clitocybe nebularis, induces maturation and activation of dendritic cells via the toll-like receptor 4 pathway. Immunology 134(4):409–418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Ismaya WT, Yunita, Efthyani A, Lai X, Retnoningrum DS, Rachmawati H, Dijkstra BW, Tjandrawinata RR (2016) A novel immune-tolerable and permeable lectin-like protein from mushroom Agaricus bisporus. Biochem Biophys Res Commun 473:1090–1093

    Article  CAS  PubMed  Google Scholar 

  8. Ismaya WT, Tandrasasmita OM, Sundari S, Diana, Lai X, Retnoningrum DS, Dijkstra BW, Tjandrawinata RR, Rachmawati H (2017) The light subunit of mushroom Agaricus bisporus tyrosinase: its biological characteristics and implications. Int J Biol Macromol 102:308–314

    Article  CAS  PubMed  Google Scholar 

  9. Ismaya WT, Tjandrawinata RR, Rachmawati H (2020) Lectins from the edible mushroom Agaricus bisporus and their therapeutic potentials. Molecules 25:2368. https://doi.org/10.3390/molecules25102368

  10. Rachmawati H, Sundari S, Nabila N, Tandrasasmita OM, Amalia R, Siahaan TJ, Tjandrawinata RR, Ismaya WT (2019) Orf239342 from the mushroom Agaricus bisporus is a mannose binding protein. Biochem Biophys Res Commun 515(1):99–103

    Article  CAS  PubMed  Google Scholar 

  11. Cummings RD, Schnaar RL (2017) Chapter 28 R-type lectins. In: Varki A, Esko RDC JD, Stanley P, Hart GW, Aebi M, Darvill AG, Kinoshita T, Packer NH, Prestegard JH, Schnaar RL, Seeberger PH (eds) Essentials of glycobiology, 3rd edn. Cold Spring Harbor, New York

  12. Hazes B (1996) The (QxW)3 domain: a flexible lectin scaffold. Prot Sci 5:1490–1501

    Article  CAS  Google Scholar 

  13. Notova S, Bonnardel Fo L, Fdr, Varrot A, Imberty A (2020) Structure and engineering of tandem repeat lectins. Curr Opin Struct Biol 62:39–47. doi:https://doi.org/10.1016/j.sbi.2019.11.006

    Article  CAS  PubMed  Google Scholar 

  14. Zhang F, Hoque MM, Jiang J, Suzuki K, Tsunoda M, Takeda Y, Ito Y, Kawai G, Tanaka H, Takenaka A (2014) The characteristic structure of anti-HIV actinohivin in complex with three HMTG D1 chains of HIV-gp120. ChemBioChem 15:2766–2773

    Article  CAS  PubMed  Google Scholar 

  15. Lai X, Soler-Lopez M, Ismaya WT, Wichers HJ, Dijkstra BW (2016) Crystal structure of recombinant MtaL at 1.35 Angstrom resolution. Acta Crystallogr F 72:244–250

    Article  CAS  Google Scholar 

  16. Pohleven J, Renko M, Magister S, Smith DF, Kunzler M, Strukelj B, Turk D, Kos J, Sabotic J (2012) Bivalent carbohydrate binding is required for biological activity of Clitocybe nebularis lectin (CNL), the N-N’-diacetylactosediamine (GalNacb1-4GlcNAc, LacdiNAc)-specific lectin from basidiomycete C. nebularis. J Biol Chem 287:10602–10612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D 66(4):486–501. doi:https://doi.org/10.1107/S0907444910007493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. DeLano WL (2008) The PyMOL molecular graphics system. Delano Scientific LLC, Palo Alto

    Google Scholar 

  19. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, Olson AJ (2009) Autodock4 and AutoDockTools4: automated docking with selective receptor flexiblity. J Comput Chem 16:2785–2791

    Article  Google Scholar 

  20. Ismaya WT, Yunita, Damayanti S, Caroline, Tjandrawinata RR, Retnoningrum DS, Rachmawati H (2016) In silico study to develop a lectin-like protein from mushroom Agaricus bisporus for pharmaceutical application. Sci Pharm 84:203–217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Trott O, Olson AJ (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31(2):455–461

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Wilm FS, Dineen A, Gibson D, Karplus TJ, Li K, Lopez W, McWilliam R, Remmert H, Söding M, Thompson J JD, D.G. H (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539. doi:https://doi.org/10.1038/msb.2011.75

    Article  PubMed  PubMed Central  Google Scholar 

  23. Kimura R, Aumpuchin P, Hamaue S, Shimomura T, Kikuchi T (2020) Analyses of the folding sites of irregular β- trefoil fold proteins through sequence- based techniques and Gō-model simulations. BMC Mol Cell Biol 21:28–44. doi:https://doi.org/10.1186/s12860-020-00271-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Diana, Ismaya WT, Meidianto VF, Tandrasasmita OM, Tjandrawinata RR, Rachmawati H (2018) Bioconjugation of captopril-light subunit of Agaricus bisporus mushroom tyrosinase: Characterization and potential use as a drug carrier for oral delivery. Biol Pharm Bull 41(12):1837–1842. https://doi.org/10.1248/bpb.b18-00553

    Article  PubMed  Google Scholar 

  25. Nakamura T, Tonozuka T, Ide A, Yuzawa T, Oguma K, Nishikawa A (2008) Sugar-binding sites of the HA1 subcomponent of Clostridium botulinum type C progenitor toxin. J Mol Biol 376:854–867. https://doi.org/10.1016/j.jmb.2007.12.031

    Article  CAS  PubMed  Google Scholar 

  26. Marquesa MRF, Barracco MA (2000) Lectins, as non-self-recognition factors, in crustaceans. Aquaculture 191:23–44

    Article  Google Scholar 

  27. Swaminathan CP, Gupta D, Sharma V, Surolia A (1997) Effect of substituents on the thermodynamics of d-galactopyranoside binding to winged bean (Psophocarpus tetragonolobus) basic lectin†. Biochemistry 36:13428–13434

    Article  CAS  PubMed  Google Scholar 

  28. Cummings RD, Schnaar RL (2017) Chapter 31 C-type lectins. In: Varki A, Esko RDC JD, Stanley P, Hart GW, Aebi M, Darvill AG, Kinoshita T, Packer NH, Prestegard JH, Schnaar RL, Seeberger PH (eds) Essentials of glycobiology, 3rd edn. Cold Spring Harbor, New York

  29. Hu Z, Wang Y, Cheng C, He Y (2019) Structural basis of the pH-dependent conformational change of the N- T terminal region of human mannose receptor/CD206. J Struct Biol 208:107384–107391

    Article  CAS  PubMed  Google Scholar 

  30. Murzin AG, Lesk AM, Chothia C (1992) Beta-Trefoil fold. Patterns of structure and sequence in the Kunitz inhibitors interleukins-1 beta and 1 alpha and fibroblast growth factors. J Mol Biol 223(2):531–543

    Article  CAS  PubMed  Google Scholar 

  31. Kirioka T, Aumpuchin P (2017) Detection of folding sites of β-trefoil fold proteins based on amino acid sequence analyses and structure-based sequence alignment. J Proteomics Bioinform 10:222–235. https://doi.org/10.4172/jpb.1000446

    Article  Google Scholar 

Download references

Acknowledgements

The works were funded by The Ministry of Research and Higher Education coordinated by The Higher Education Excellent Research through the Program Unggulan Perguruan Tinggi (2020) and supported by Dexa Medica.

Author information

Authors and Affiliations

  1. Dexa Laboratories of Biomolecular Sciences, Industri Selatan V, PP-7, 17550, Cikarang, Indonesia

    Wangsa Tirta Ismaya & Raymond Rubianto Tjandrawinata

  2. Research Group of Pharmaceutics, School of Pharmacy, Bandung Institute of Technology, Ganesa 10, 40132, Bandung, Indonesia

    Heni Rachmawati

  3. Research Center for Nanosciences and Nanotechnology, Bandung Institute of Technology, Ganesa 10, 40132, Bandung, Indonesia

    Heni Rachmawati

Authors
  1. Wangsa Tirta Ismaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Raymond Rubianto Tjandrawinata
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Heni Rachmawati
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Wangsa Tirta Ismaya or Heni Rachmawati.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ismaya, W.T., Tjandrawinata, R.R. & Rachmawati, H. Prediction of the Mannose-Binding Site in the Agaricus bisporus Mannose-Binding Protein. Protein J 40, 554–561 (2021). https://doi.org/10.1007/s10930-021-09993-6

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10930-021-09993-6

Keywords

Search

Navigation